Energy &
Environmental
Science
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
PERSPECTIVE
View Journal
Cite this: DOI: 10.1039/c5ee01167a
Oxygen-tolerant proton reduction catalysis: much
O2 about nothing?†
David W. Wakerley and Erwin Reisner*
Proton reduction catalysts are an integral component of artificial photosynthetic systems for the
production of H2. This perspective covers such catalysts with respect to their tolerance towards the
potential catalyst inhibitor O2. O2 is abundant in our atmosphere and generated as a by-product during
the water splitting process, therefore maintaining proton reduction activity in the presence of O2 is
Received 14th April 2015,
Accepted 29th May 2015
important for the widespread production of H2. This perspective article summarises viable strategies for
DOI: 10.1039/c5ee01167a
future research. H2-evolving enzymatic systems, molecular synthetic catalysts and catalytic surfaces are
www.rsc.org/ees
catalysts can be studied are described.
avoiding the adverse effects of aerobic environments to encourage their adoption and improvement in
discussed with respect to their interaction with O2 and analytical techniques through which O2-tolerant
Broader context
The generation of hydrogen from water is a potential approach to develop a clean and renewable fuel. This process is carried out by proton reduction catalysts
and currently research is focussed on the development of efficient and robust catalytic species. Application of the water-splitting process will be carried out on a
large scale, not restricted to the laboratory, and as such it is necessary to consider how O2 in our atmosphere or produced as a side product from water splitting
would interact with such an arrangement. O2 is an inhibitor of a number of catalytic processes and therefore designing strategies to avoid O2 inhibition is
crucial in the production of viable proton reduction systems.
1. Introduction
The large scale production of H2 through artificial photosynthesis
stands as an aspiring goal of contemporary science.1–3 Chemicalenergy storage through water splitting generates both H2 and O2 and
relies on efficient reduction and oxidation catalysts, respectively
[reaction (1)].
H2O - H2 +
1
2
O2
DE0 = 1.23 V
(1)
Research into viable catalysts is consequently gathering significant
interest,4 but there remain several limitations that must be
addressed before such systems can be implemented on a
commercial scale. For example, avoiding non-aqueous solutions,
increasing long-term stability and sustaining high catalytic efficiency
are all goals for a benchmark catalyst and progress in these areas has
proceeded at an appreciable rate.
Christian Doppler Laboratory for Sustainable SynGas Chemistry, Department of
Chemistry, University of Cambridge, Lensfield Road, Cambridge CB2 1EW, UK.
E-mail: [email protected]; Web: http://www-reisner.ch.cam.ac.uk/
† Electronic supplementary information (ESI) available: Data used to prepare
Fig. 3. See DOI: 10.1039/c5ee01167a
This journal is © The Royal Society of Chemistry 2015
One issue that remains relatively underexplored is the
impact of O2 on synthetic proton-reducing systems. Less than
a decade ago it seemed common sense that synthetic molecular
H2-evolving catalysts would operate poorly under air due to the
propensity of O2 to irreversibly damage a catalytic structure
during turnover. As a result, research was carried out under
inert atmospheres of N2 or Ar. Given that the end goal for a proton
reduction catalyst would be its widespread use in a H2-fuelled
economy, any observable O2-sensitivity would seriously impair its
practicality. Adding to this, stringent anaerobic conditions are
costly to maintain on an industrial scale. Developing catalysts that
could operate under O2 consequently stood as a major challenge
for H2 production research,5,6 yet recent publications have demonstrated that avoiding the inhibiting effects of O2 may be more
manageable than first imagined and O2-tolerant proton reduction
is now a fast-developing field.
Exposure of a proton reduction catalyst to O2 in a water
splitting system, particularly over prolonged periods of time, is
almost unavoidable. Fig. 1a shows a standard electrolyser/
photoelectrochemical (PEC) cell, which contains an O2 evolving
anode and a H2 producing cathode separated by a proton
exchange membrane to prevent crossover of the evolved gaseous
products.7 Interaction between O2 and the proton reducing
Energy Environ. Sci.
View Article Online
Perspective
Energy & Environmental Science
potentials have on O2. In a pH 7 solution there are a number of
potential O2 reduction reactions that could occur, many of
which form reactive oxygen species (ROS):17
Water formation:
O2 + 4H+ + 4e - 2H2O
7 00
E
= +0.82 V
(2)
7 00
= +0.28 V
(3)
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
ROS formation:
O2 + 2H+ + 2e - H2O2
O2 + e - O2 E
7 00
= 0.33 V
E
H2O2 + H+ + e - HO + H2O
(4)
7 00
E
= +0.38 V
(5)
7 00
= +1.35 V
(6)
ROS reduction
H2O2 + 2H+ + 2e - 2H2O
HO + H + e - H2O
Fig. 1 Potential routes through which a proton reducing catalyst could be
exposed to O2 in (a) a standard electrolysis/PEC cell, (b) an artificial leaf and
(c) photocatalytic water-splitting particles.
+
E
7 00
E
O2 + 2H+ + e - H2O2
= +2.32 V
7 00
E
= +0.89 V
(7)
(8)
Proton reduction:
cathode can still occur through O2 leakage from the atmosphere
into the electrochemical cell or from the anodic chamber after
membrane degradation.8,9 Another configuration is the ‘artificial
leaf’,10,11 a simplification of which can be seen in Fig. 1b. The
cathode and anode are attached on opposing sides of a photovoltaic
layer that drives catalysis and some exposure of the proton reduction
catalyst to O2 is inherent in the system’s design. Photocatalytic watersplitting particles are also a promising route to full water splitting,
see Fig. 1c.12,13 H2 and O2 are produced on the same or a
neighbouring light-absorbing particle, which is often loaded with a
catalyst to enhance catalysis. The close proximity of O2 and H2
evolution sites makes interaction between catalyst and O2 inevitable
without additional protection of the catalyst.
Contemporary research has started to cover the concept of
O2-tolerant H2 generation to realise systems in which the presence of
O2 is inconsequential. This field is still in its infancy, nonetheless the
reported O2-tolerant systems present innovative routes to efficient,
aerobic proton reduction. Broadly speaking the current examples fall
into one of three areas of catalyst: proton reducing enzymes (hydrogenases),14 molecular complexes5 and catalytic surfaces.15,16
In this perspective, each of these examples will be discussed
to encourage a holistic development of O2-tolerant catalyst
systems. A discussion of the electrochemical/spectroscopic study
of O2-tolerance is also provided to highlight key techniques that
will be vital for fully understanding the effects of O2 on a proton
reduction system.
2H+ + 2e - H2
7 00
E
= –0.41 V
(9)
Potentials stated vs. NHE
Direct O2 reduction to water through reaction (2) forms the most
thermodynamically stable product, but the process is kinetically
slow due to the high dissociation energy of the dioxygen bond,18
which has a considerable thermodynamic barrier of 498 kJ mol1.
The reduction also requires 4e and 4H+ and therefore, with the
exception of a few highly active catalytic sites, it is much more likely
that incomplete O2 reduction occurs to form H2O2, O2 or OH if
sufficiently reducing conditions are available [reactions (3) to (5)].
These species can subsequently be reduced to water in a multi-step
reaction sequence [reactions (6) to (8)].
Each of the O2-reduction reactions (2) to (8) occurs at a less
negative potential than the proton reduction reaction (9), which
implies that any system capable of reducing protons will have
sufficient driving force for O2 reduction to either generate water
or ROS. It should be noted that photochemical systems may
also generate reactive singlet O2 (1O2) through triplet–triplet
annihilation. The interaction of a H2 evolving catalyst with O2
has two potential outcomes: O2-tolerant proton reduction or
inhibited catalysis due to O2-sensitivity (Fig. 2).
Oxygen-sensitive catalyst
O2-sensitive proton reduction catalysts undergo a critical drop
in H2 production activity in the presence of O2. In this case the
catalyst is susceptible to deactivation by reaction with O2 or
2. Oxygen in a proton reducing system
Proton reduction is a pH dependent redox process that has a
formal redox potential, E0 0 , of 0 (pH 59) mV vs. the normal
hydrogen electrode (NHE) (25 1C). Applied potentials more
negative than E0 0 are needed to drive H2 evolution and under
aerobic conditions it is necessary to consider the effect such
Energy Environ. Sci.
Fig. 2
Two routes through which O2 can affect catalytic proton reduction.
This journal is © The Royal Society of Chemistry 2015
View Article Online
Energy & Environmental Science
Perspective
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
with the ROS produced in reactions (3)–(5) or (8). The reducing
sites at which O2 or ROS attack are typically essential to proton
reduction activity and therefore the catalyst is irreversibly
inhibited.
O2-sensitive catalysts require a defensive approach to overcome
irreversible O2 inhibition (see below). This involves protecting a
catalyst from exposure to O2/ROS in order to generate a locally
anaerobic environment.
Oxygen-tolerant catalyst
O2-tolerance is a term used to describe a catalyst that maintains
a degree of activity in the presence of O2. In this case the
catalyst is able to reduce the incoming O2 or ROS without being
irreversibly damaged. Proton reduction is therefore in competition
with O2 reduction and H2 is often produced at a decreased rate and
efficiency under aerobic conditions.
The reduction of O2 by O2-tolerant catalysts can be seen as
an offensive approach to prevent O2-inhibition. The catalyst is able
to remove O2 as a threat and allows H2 evolution to continue.
Designing a proton reduction catalyst capable of reducing O2 and
ROS to harmless by-products is an elegant strategy to realise
aerobic proton reduction. O2-tolerance can be enhanced further
through design of a catalyst that has favourable kinetics for proton
reduction over O2 reduction.
3. Analytical techniques to study
oxygen tolerance
Studying the O2 tolerance of a proton reducing species is a
relatively new line of research and as such, routine analytical
techniques are not commonplace in most laboratories. Currently,
electrochemistry offers the simplest and most effective approach.
Analysis of currents stemming from a catalyst and quantification of
the H2 produced can be used to calculate turnover frequencies
(TOFs),19 turnover numbers (TONs) and determine redox processes
under O2.20 These techniques can be applied across all types of
H2-evolving catalysts.
Cyclic voltammetry (CV) offers a fast method to study redox
changes and catalytic currents. CV analysis starts from a catalyticallyinert potential and scans to a more negative potential at which
clear proton reduction currents are observable. The onset of
proton reduction and size of the reduction wave, along with
Tafel slope analysis, provide a measure of a catalyst’s activity.
The first step in the study of O2 tolerance is to establish
whether this activity changes under aerobic conditions. If a
catalyst is O2 sensitive, a CV in air will result in a significant
drop in proton reduction current, whereas little change in the proton
reduction wave indicates O2-tolerant catalysis. An O2-tolerant catalyst
may also display an O2 reduction wave, demonstrating simultaneous
proton/O2 reduction. O2 tolerance is visible on a Pt electrode, where
an O2 reduction wave (onset +0.5 V vs. NHE) can be observed under
an O2 atmosphere, whilst the proton reduction wave (onset around
0.4 V) is maintained (Fig. 3). CV only gives an indication of
O2-tolerance on a short time-scale, and analysis must therefore
be supplemented with other techniques.
This journal is © The Royal Society of Chemistry 2015
Fig. 3 Cyclic voltammograms on a Pt disk electrode in phosphate buffer
(pH 7, 0.1 M) under aerobic and anaerobic conditions under N2 at a scan
rate of 50 mV s1 at room temperature.21 The anodic wave can be
attributed to the oxidation of H2 generated during the cathodic scan.
Controlled potential electrolysis (CPE) is another vital tool in
the study of proton reduction catalysis. In this process a constant
potential is applied to a catalyst, allowing measurable quantities
of H2 to build up that can be quantified through techniques such
as gas chromatography. Confirming that H2 has been produced
under aerobic conditions is of paramount importance, as otherwise it is not clear if an observed current stems from H2
evolution or O2/ROS reduction. Quantification of H2 also allows
the Faradaic efficiency (FE) to be calculated. FE is a measure of
the electrons used vs. the H2 produced and would be 100% if all
electrons were consumed for proton reduction. Quantification of
the H2 produced and FE from CPE under aerobic and anaerobic
atmospheres gives a clear indication of a catalyst’s O2 tolerance
and selectivity for proton reduction over O2 reduction. CPE is
also necessary to establish long-term catalytic stability under O2,
as inhibition may occur over prolonged O2/ROS exposure. Such
experiments may be further extended to include the effect of
varying levels of O2 on catalysis.
Interaction between photocatalysts and O2 may also be
studied using surface photovoltage spectroscopy. This technique
monitors the contact potential difference as a function of photon
energy in order to determine the surface states and energy
necessary for O2 reduction on a given substrate.22
At present, analysis of O2-tolerance is confined to measuring
the H2 produced by a catalyst with and without O2, however this
should be coupled with analysis of the formed ROS to gain a
complete appreciation of the catalyst’s aerobic activity. Rotating
ring-disk electrochemistry is one of the most common methods
of ROS detection, which can distinguish the production of H2O2 vs.
H2O. This technique requires a disk electrode, consisting of the
catalyst to be studied, encircled by an electrode ring, which is
typically Pt. When this electrode is rotated there is laminar flow
of solution from the central disk to the outer ring electrode.20 By
holding the ring at oxidizing potentials with a bipotentiostat, it is
possible to detect products from O2 and H+ reduction through
their unique redox potentials. This technique can be used to
monitor the production of H2O2 or H2,23 which can determine
the degree of selectivity and O2-tolerance of a given proton
reduction catalyst.24
Energy Environ. Sci.
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Perspective
Energy & Environmental Science
A range of electrochemical sensors can similarly be implemented
to detect the formation of ROS. Detection of O2 has been achieved
by a number of protein-based electrodes, such as those loaded with
superoxide dismutase25–27 or cytochrome c28,29 and more recently,
protein-free detectors have been utilised.30–32 Similarly H2O2 can
be detected through attachment of horseradish peroxidase,33
cytochrome c34 or CuS35 to an electrode. This subject has recently
been reviewed.36
ROS detection can also be achieved through the measurement
of a unique spectroscopic signal, such as the UV peak of H2O237
and mass-spectrometry allows the quantification of 18O2 reduction
to H218O. Alternatively, spectroscopic probes can be used, which
can specifically determine nM concentrations of a given ROS.38
Spectroscopic probing of the catalyst during proton reduction is
equally important in order to visualise the structural and electronic
changes that lead to O2-sensitivity and tolerance. Through such
analysis a complete appreciation for ROS/H2 formed at a given
applied potential vs. current expended can be realised, allowing
conclusions concerning the interaction of the catalyst with O2 to
be drawn.
4. Oxygen-tolerant hydrogenases
Hydrogenases are nature’s H2-cycling catalysts and display a
high ‘per active site’ activity with TOFs up to 104 s1, rivalling
that of Pt.39,40 These enzymes consist of well-suited structures
to undertake proton reduction/H2 oxidation and as such have
received much attention.14 [NiFe] and [FeFe] hydrogenases,
categorised according to their active site composition, are the
two classes of hydrogenases capable of proton reduction to H2.
In each hydrogenase the active metal ions are ligated by CN,
CO and cysteine ligands and are typically connected to the
protein exterior via iron–sulphur clusters. The disadvantages to
the use of hydrogenases include difficult and costly purification,
fragility, a large catalyst footprint (high ‘volume per active site’
ratio) and an infamous sensitivity to small quantities of O2.
Hydrogenase interaction with O2 is a considerably wellestablished area of research and may be instrumental in
engineering O2-tolerant synthetic systems.41 In-depth electrochemical and spectroscopic studies have illustrated the route to
O2 inhibition across a range of hydrogenases and this work has
been reviewed a number of times.14,42 As such this perspective
will only briefly summarise the interaction between hydrogenases and O2 and instead focus on emerging strategies to shield
the enzyme from aerobic atmospheres.
Both classes of hydrogenase consist of a range of subclasses
and the O2 susceptibility of each depends to some extent on
the environment in which the enzyme functions biologically.
Generally, both the [NiFe] and [FeFe] hydrogenases are inhibited
by O2 due to their interaction with ROS. Upon exposure of a
[FeFe] hydrogenase to air, the active site, known as the H-cluster,
is believed to form a ROS, which oxidises its proximal [4Fe–4S]
cluster and prevents electron transfer through the enzyme to
the active site.44 [NiFe] hydrogenases deactivate through the
reduction of O2 to form an oxidised and paramagnetic ‘unready’
Energy Environ. Sci.
Fig. 4 (a) Schematic representation of the formation and recovery of the
oxidised Ni-A and Ni-B states in the [NiFe] hydrogenase active site
(adapted from ref. 43). (b) Active site of the [NiFeSe] hydrogenase and
two reported oxidised structures from Desulfomicrobium baculatum
(Ox4B state) and Desulfovibrio vulgaris (conformer I).
Ni-A state of the active site that is slow to reactivate45 (see Fig. 4a).
The exact form of this state is debated, but crystallographic studies
have suggested that a hydroperoxo ligand is ligated to the Ni ion as
a result of incomplete O2 reduction.46
The concept of O2-tolerant H2 oxidation has become an
exciting branch of research, in particular for the membranebound [NiFe] hydrogenase from Ralstonia eutropha, which can
oxidise H2 under atmospheric levels of O2.47–49 O2-tolerant
hydrogenases are more likely to form a paramagnetic Ni-B (or
‘ready’) state upon exposure to O2, as a result of more complete
O2 reduction to form a bridging hydroxo ligand.46 The route to
their tolerance is believed to originate from six cysteine residues
surrounding the unique proximal [4Fe–3S] cluster next to the
enzyme’s active site.50 The cysteines facilitate structural changes
that allow the cluster to transfer two electrons within a small
potential range.51,52 When O2 enters the active site, one electron
from the reduced Ni and two from the proximal [4Fe–3S] cluster
allow the hydrogenase to consistently form the Ni-B state
(Fig. 4a), which very quickly reactivates (t o 1 min). Recent
evidence has suggested that conversion from Ni-A to Ni-B may
occur through the oxygenation of one of the bridging S-atoms.53
Despite promising O2-tolerance, this exceptional type of [NiFe]
hydrogenase is biased towards H2 oxidation over proton reduction
and is inhibited by H2.42
The [NiFeSe] hydrogenase is a subclass of the [NiFe] hydrogenase that is highly active for proton reduction in the presence
This journal is © The Royal Society of Chemistry 2015
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Energy & Environmental Science
of H2 and illustrates a promising degree of tolerance to O2.14
[NiFeSe] hydrogenases contain a ligated selenocysteine moiety
in place of one of the terminal cysteines of the conventional
[NiFe] enzyme (Fig. 4). O2 exposure of the enzyme does not form
substantial quantities of Ni-A/Ni-B states as a paramagnetic
NiIII is not observed.54 The major products from oxidation of
two [NiFeSe] hydrogenases are presented in Fig. 4b. The active
site from Desulfomicrobium baculatum when crystallised aerobically
contains an oxidised selenocysteine moiety (referred to as Ox4B)54
and the Desulfovibrio vulgaris species, when purified and crystallised
aerobically, contains an oxidised Se and doubly-oxidised S
(referred to as conformer I).55,56 The chemical role of selenocysteine in protecting the hydrogenase from oxidative damage
is currently under investigation,57 but it has been shown that
the [NiFeSe] hydrogenase is able to reactivate faster under
anaerobic conditions after O2-exposure in comparison to the
O2-sensitive [NiFe] species.58 The O2 tolerance may be a result
of the easier redox chemistry of Se compared to S.59
Due to the extreme O2 sensitivity of many hydrogenases,
engineering the enzymes to reduce protons and O2 simultaneously
is a significant challenge,60,61 and currently more practicable
approaches to aerobic H2-evolution involve shielding the enzyme
from exposure to O2. This involves a ‘retrofitted’ O2-defending
shield that reduces O2 before it can have adverse effects on enzyme
activity. To date, ‘shields’ have been predominantly based on
photochemical systems that remove O2 from a system during
irradiation.
In 2009 we reported that Desulfomicrobium baculatum [NiFeSe]
hydrogenase attached to a Ru-sensitised TiO2 nanoparticle was
able to produce H2 photocatalytically in a N2 purged vial outside
a glovebox.64 Although this sacrificial photosystem sustains H2
generation under traces of O2, it cannot maintain photo-H2
Perspective
production activity under atmospheric O2 levels due to the lack
of efficient O2 shielding and presumably enzyme-damaging ROS
formation on irradiated TiO2 in the presence of O2 (see Section 5).
Peters and coworkers showed in 2012 that a [NiFe] hydrogenase from Thiocapsa roseopersicina covalently linked to a Ru
dye was able to photocatalytically reduce protons under aerobic
conditions in the presence of the soluble redox mediator methyl
viologen (MV) and a sacrificial electron donor.65 Under an aerobic
atmosphere and an initial lag period, where presumably dissolved
O2 was photo-reduced, this system generated H2 at 11% of the
initial rate observed under pseudo-inert conditions. An analogous
system that used a Ru dye, which was not linked to the enzyme,
showed no activity under air. It was therefore concluded that by
attaching the Ru dye to the hydrogenase a local concentration of
reduced MV was generated around the hydrogenase, which
reduced O2 before it reached the enzyme and partially shielded it
from inhibition.
Another example of O2-shielding came in 2013,62 when we
reported photocatalytic H2 production with a Desulfomicrobium
baculatum [NiFeSe] hydrogenase and the organic dye eosin Y in
the presence of a sacrificial electron donor (Fig. 5a). The
photoactivity of this mediator-free system was tested under
increasing concentrations of O2 and it was able to maintain a
notable degree of photocatalytic activity. Even under 21% O2,
10% of the enzyme’s activity (corresponding to a TOF of 1.5 s1)
was sustained relative to the anaerobic experiment, without the
observation of a significant lag phase to start H2 production.
Excited eosin Y promotes proton reduction, reduction of O2 and
conversion of O2 to 1O2.66 The O2-tolerance of the system may
therefore stem from the photo-reduction of O2 and fast formation
of 1O2 by the dye, which presumably reacts with eosin Y or the
electron donor to create an anaerobic environment (Fig. 5a).
Fig. 5 (a) Photo-excited eosin Y as a shield to protect a [NiFeSe] hydrogenase.62 (b) O2-shielding strategy based on a multi-component system
consisting of a Ru dye, methyl viologen as soluble redox mediator and a hydrogenase in nanoporous glass. Reduced methyl viologen is generated upon
photo-excitation of the dye and used to reduce the hydrogenase and quench O2 inside the pores to produce an anaerobic environment.63 The sacrificial
electron donor used to quench the dye omitted for clarity in (a) and (b).
This journal is © The Royal Society of Chemistry 2015
Energy Environ. Sci.
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Perspective
The concept of shielding has been extended by Dewa and
coworkers in 2014 through the implementation of porous
enzyme-immobilising frameworks.63 In this case, a nanoporous
glass plate was soaked in a tris(bipyridine)rutheniumII dye,
MV and a [NiFe] hydrogenase from Desulfovibrio vulgaris. The
nanoporous framework consisted of 50 nm channels that
directed diffusion of O2 into the structure. The MV reduced
O2 in the channels as it entered the glass during irradiation,
producing a shielded pathway that allowed protons to reach the
hydrogenase but not O2 (Fig. 5b). The glass framework thereby
allowed sacrificial H2 evolution to be powered photocatalytically through the Ru dye. The system was able to generate H2 at
photocatalytic rates as high as 7.9 s1 per enzyme, with a TON
of 130 000 over 12 hours under aerobic atmospheres.
Shielding strategies have also been applied to H2 oxidising
systems. Redox active polymers containing viologen moieties
are capable of simultaneously immobilising and protecting
hydrogenases during H2 oxidation,67,68 and 3D porous carbon
electrodes loaded with hydrogenase have sustained H2 oxidation activity by favouring the effusion of H2 over O2.69 These
approaches could also be employed for H2 evolving systems.
Despite being complex and multifaceted, the interaction
between hydrogenases and O2 is generally thoroughly investigated.
Yet there is currently enormous scope for the development of
improved O2 shielding systems and scaffolds to protect the enzyme
and allow the use of more O2-sensitive hydrogenases in less stringent
environments. Future work should remove redox mediators and
sacrificial agents from these systems and focus on constructing O2
shields on hydrogenase-modified electrodes to retroactively produce
O2-tolerant hydrogenase systems.
5. Oxygen-tolerant molecular
synthetic catalysts
Synthetic molecular catalysts are discrete transition metal
complexes consisting of metal/ligand combinations designed to
promote proton reduction.4,70 Study of their activity is normally
restricted to the homogeneous phase, containing the dissolved
catalyst and an electron source, which is typically an electrode, a
dye with a sacrificial electron donor or a strong chemical reducing
agent. Recent examples have shown innovative rational design71–75
and the field has been reviewed numerous times.5,76 These catalysts
do not typically exhibit TONs or TOFs comparable to hydrogenases
and the most active solid-state catalysts, but offer a defined catalytic
site that can be easily manipulated and used to establish functionality and mechanisms that are essential for efficient proton
reduction activity.
Molecular catalysts are often inspired by the active site of
hydrogenases and are frequently referred to as ‘artificial hydrogenases’ accordingly.77 Due to the low tolerance of hydrogenases
towards O2, for a long time molecular catalysts were assumed to
be unusable under aerobic conditions,5 however it is becoming
increasingly apparent that molecular synthetic catalysts do not
necessarily exhibit the debilitating O2-sensitivity of the enzymes
they mimic.
Energy Environ. Sci.
Energy & Environmental Science
Fig. 6 Currently known Co-based O2-tolerant molecular proton reduction
catalysts. 1A: water-soluble cobaloxime;78 1B: fluorinated Co corrole;80 1C:
acetylated Co microperoxidase-11;81 1D/1E: Co polypyridyl catalysts.82,83
Our group reported the first full study of O2-tolerant proton
reduction with a synthetic molecular complex.78 The study used
a water-soluble [Et3NH][CoIIICl(dimethylglyoximato)2(pyridyl-4hydrophosphonate)] catalyst (Fig. 6 shows fully protonated
complex 1A) and explored changes in activity under varying
levels of O2. CVs of the catalyst were undertaken under N2, O2
and CO (Fig. 7).79 Catalytic currents were seen under N2 and O2
(Fig. 7a) but not CO, a known catalyst inhibitor (Fig. 7b). The
large difference in proton reduction current between the COinhibited CV and the aerobic CV illustrates the O2-tolerant
activity of the complex. Evidence of O2 reduction was also
visible as the non-catalytic CoII/CoIII oxidation wave from the
cobaloxime was not seen under aerobic conditions and the size
of the CoIII/CoII wave increased, indicating competitive O2
reduction by the cobaloxime in the CoII oxidation state (Fig. 7a).
Subsequent CPE of this complex under inert and aerobic
conditions at Eappl = 0.7 V vs. NHE (0.29 V overpotential)
showed that substantial H2 production activity remained in the
presence of O2. After re-purging the aerobic catalyst solution
with N2 and repeating CPE, the cobaloxime regained 100% of
its initial activity, suggesting the drop in activity under air was a
result of competitive O2 reduction by the cobaloxime and not
O2 sensitivity.
Photochemical experiments supported this result. Catalysis
was driven photochemically using either a heterogeneous
Ru-photosensitised TiO2 nanoparticle system or a homogeneous
dye, eosin Y, and the evolved H2 was measured under increasing
concentrations of O2. Under 21% O2, 71% of the original H2
evolution activity was measured in the homogenous system and
This journal is © The Royal Society of Chemistry 2015
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Energy & Environmental Science
Fig. 7 CVs of 1A (1 mM) in 0.1 M triethanolamine/Na2SO4 at pH 7 under
atmospheres of (a) N2 and air and (b) N2 and CO. Scan rate was 100 mV s1
on a glassy carbon working electrode. Taken from ref. 79.
17% was maintained in the colloidal system, which illustrated
the O2 tolerance of the cobaloxime complex. Subsequent experiments with other cobaloxime variants have shown similar levels
of O2 tolerance.24,84
It should be noted that the degree of O2 tolerance exhibited
by 1A varied depending on the electron source and as such the
dye or electrode and the correspondingly applied potential to
the catalyst must be considered when studying molecular
systems under O2. Most commonly used electrodes are capable
of reducing O2 to some extent and any currents stemming from
a homogeneous catalyst must be deconvoluted from this background electrode activity. CVs of glassy carbon in air show a
wave at 0.5 V vs. NHE in pH 7 solution (Fig. 7a, background)
and FEs of a catalyst will typically be significantly less than the
expected 100% for the same reason.79 The photosensitiser will also
react with O2 during catalysis, lowering the rate of electron transfer
to the catalyst and producing ROS. Organic dyes, such as fluorescein,
rose bengal and eosin Y are common photosensitisers due to their
appealing lack of precious metal centre, however under O2 they are a
source of 1O2,66 which will rapidly react with catalyst ligands.
Ruthenium polypyridine dyes are similarly quenched by O2.85 These
dyes can be coupled to TiO2 to assist in charge separation, however
the TiO2 is capable of producing ROS in the form of O2 and OOH
during irradiation.86 The low activity of the heterogeneous TiO2based system that drove photocatalysis of 1A could be a result of
O2 formation with concomitant desorption or decomposition of
the Ru dye or catalyst.87
Following on from the cobaloxime system, a Co corrole
catalyst synthesised by the Dey group demonstrated similar
levels of O2 tolerance in 2013 (1B, Fig. 6).80 The study used a
fluorinated macrocycle to decrease the overpotential needed for
proton reduction and catalytic activity was established using a
rotating ring-disk electrode consisting of the complex immobilised
on an edge plane graphitic electrode with a Pt ring. Rotating ringdisk experiments were carried out in the presence of O2, allowing
the authors to analyse the O2 reduction by the Co corrole through
oxidation of the generated H2O2. This demonstrated the real time
reduction of protons to H2 under aerobic conditions by the catalyst
and CPE gave a FE of 52% under air after 10 hours of electrolysis in
0.5 M H2SO4. The O2 tolerance of the Co corrole stems from its
ability to reduce O2 without deactivation, which had been reported
previously.88
This journal is © The Royal Society of Chemistry 2015
Perspective
Bren and coworkers demonstrated in 2014 that an acetylated
Co microperoxidase-11 complex (1C, Fig. 6) was O2 tolerant.81
This catalyst has a macrocyclic centre similar to that of 1B and
showed a high FE of 85% when CPE was carried out over 4 hours in
a pH 7 solution (13% lower than the equivalent experiment under
N2). The high FE seen in this case may be a result of the large
applied overpotential (850 mV), making the barrier of proton
reduction over O2 reduction less significant. In such a case the
relative concentrations of protons over O2 would determine catalyst
selectivity. At room temperature the concentration of O2 is 0.3 mM
under aerobic conditions89 with a diffusion coefficient of 2 105 cm2 s1,90 and is therefore outmatched by the highly available
and faster diffusing protons.
Cobalt polypyridyl catalysts have also demonstrated a degree
of tolerance to O2. These catalysts typically show high stability
towards deactivation and a number of structural variants have been
synthesised.91,92 [Co(N,N-bis(2-pyridinylmethyl)-2,20 -bipyridine-6methanamine)(OH2)][PF6]3 ([Co(DPA-Bpy)(OH2)][PF6]3) (1D, Fig. 6)
is an O2-tolerant Co polypyridyl complex published by Zhao and
coworkers.82 Using a [Ru(bpy)3]2+ photosensitiser in the presence
of ascorbic acid as a sacrificial electron donor, the catalyst retained
40% of its activity in the presence of air, however this was not
explored in more detail. This has been followed up by Lloret-Fillol
and coworkers who used a 1,4-di(picolyl)-7-( p-toluenesulfonyl)1,4,7-triazacyclononane (Py2TStacn) ligand to form a Co complex
capable of generating H2 under O2 (1E, Fig. 6).83 In this case 25%
of catalytic activity was maintained under air using a molecular Ir
photosensitiser.
The O2-tolerant catalysts discussed thus far have a similar
structure, consisting of N-ligating ligands to a Co centre. Proton
reduction in such species is thought to occur through CoII/CoI
intermediates to form a CoIII–H.82,93,94 The hydridic intermediate may then reduce a proton to form H2 or be further reduced
to CoII–H, which evolves H2 (Fig. 8). Each of the reduced Co
centres could also be active for O2 reduction95,96 (Fig. 8) and there is
precedent for the formation of H2O2 by cobaloximes24,97 and H2O
by Co corroles.88 Proficient reduction of O2 and ROS to harmless
species by these catalysts may explain their limited deactivation in a
similar manner to O2-tolerant hydrogenases. The catalytic core of
these complexes is also comparable to Vitamin B12 and parallels
can be drawn between the H2 production and O2 reduction activity
of these species.96 Comparison of these complexes to biological
structures will be useful in understanding the effects of O2 inhibition in both classes of catalyst.
It is important for the study of O2-tolerant molecular complexes to move away from the Co–N based scaffold and branch
Fig. 8 The proposed mechanism for heterolytic H2 evolution from Co
complexes 1A–E and the potential O2 reduction reactions that could be
carried out at the reduced intermediates. Adapted from ref. 98.
Energy Environ. Sci.
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Perspective
Energy & Environmental Science
Fig. 9 The O2-sensitive Ni bis(diphospine) complex, 1F, and the proposed
route of inhibition. Complexes 1G and 1H are O2 tolerant square planar Ni
complexes.100
out into different ligand structures and metal centres to establish other functionalities insensitive to deactivation. A recent
study of O2 tolerance with a Ni bis(diphosphine) catalyst (1F,
Fig. 9) was consequently carried out by our group.79 The cyclic
phosphine ligand-set coordinated to Ni contains pendant
amines, which serve as proton relays that has led to high
activity in organic and aqueous solution.72,75 CV of this
hydrogenase-inspired catalyst showed little difference between
anaerobic and aerobic conditions, however CPE at 0.4 V vs.
NHE (0.13 V overpotential) at pH 4.5 produced 1.05 mmol of H2
(72% FE) under N2, but no H2 under 21% O2, indicating a high
degree of O2-sensitivity.79 In its native Ni2+ oxidation state this
catalyst is air stable, suggesting that a reduced form of the
catalyst is susceptible to reaction with ROS/O2. The inactivation
has been assigned to oxidation of the phosphine ligands to
phosphine oxides during turnover under O2 (Fig. 9), which
show no proton reduction activity. This effect has been
observed when using compounds with similar composition as
O2 reduction catalysts.99
Table 1
Recently two square planar Ni thiolate-containing complexes have shown a high degree of O2 tolerance. These
simple structures are notable for their high stability and in
a recent report Eisenberg and coworkers showed that catalysts 1G and 1H (Fig. 9) exhibited TONs of 62 000 and 80 000,
respectively, over 40 h CPE in aerobic solutions.100 CVs of the
catalysts were identical under Ar or air and CPE showed a
15–18% drop in FE between inert and aerobic conditions
(93 to 78% for 1G and 98 to 80% for 1H). The high FE suggests
that these catalysts are robust in air, which may be related to the
high overpotential applied (between 700–800 mV), much like
catalyst 1C.
To gauge the current state of O2-tolerant molecular proton
reduction catalysts, all examples known to us and their catalytic
properties are summarised in Tables 1 and 2. In an ideal
situation, H2 would be produced at mild overpotentials, with
the same rate and efficiency regardless of whether O2 is present.
This is not yet the case, however, examples continue to push the
boundaries of what was previously thought possible and it
appears that this could be realised within the next few years.
There are many other known molecular catalysts that should
be studied under O2 to establish a clear trend between catalyst
structure and O2-tolerant proton reduction. It is also important
that O2-tolerance studies are carried out in aqueous solution,
rather than commonly used organic solvents as the solubility
and behaviour of O2 in these environments is drastically
different (O2 solubility in acetonitrile = 8.1 mM at 25 1C).101
Computational studies have begun to establish the effects of O2
on a molecular catalyst structure,102 but further expansion and
comparison to experimental data is required. Future investigation must also include the study of ROS intermediates and their
interaction with metal complexes to establish the O2 reduction
tendencies of the O2-tolerant vs. the O2-sensitive catalysts.
Nevertheless, at present it would seem that choosing a molecular catalyst capable of both catalytic O2 and proton reduction
is the most viable strategy to attain an O2-tolerant molecular
system.
Summary of CPE with O2-tolerant molecular catalysts and their H2 production activity under O2
Complex
Catalyst/electrode material
TOF under
anaerobic/aerobic
atm. (h1)
1A
1B
1C
1G
1H
Cobaloxime/glassy carbon
Co corrole/graphite
Acetylated Co microperoxidase-11/Hg pool
[Ni(2-aminobenzenethiolate)2]/glassy carbon
[Ni(2-pyridinethiolate-N-oxide)2]/glassy carbon
3.68/0.83
N/A
6250/4750
N/A/1550
N/A/2000
Table 2
pH
Over-potential
(mV)
FE under
anaerobic/aerobic
atm.
Ref.
7
0
7
7
7
290
800
850
800
780
67/10 to 43%
N/A/52%
98/85%
93/78%
98/80%
78 and 79
80
81
100
100
Summary of photocatalytic systems with O2-tolerant molecular catalysts and their H2 production activity under O2
Complex
Catalyst/photosensitiser
TOF under
anaerobic/aerobic
atm. (h1)
1A
1A
1D
1E
Cobaloxime/TiO2-tris(bipyridine)Ru
Cobaloxime/eosin Y
[Co(DPA-Bpy)(OH2)][PF6]3/tris(bipyridine)Ru
[Co(CF3SO3)(Py2TStacn)][CF3SO3]/bis(2-phenylpyridine)(bipyridine)Ir
15/2.6
62.0/44.2
N/A
147/44
Energy Environ. Sci.
% Activity in
aerobic atm. (%)
pH
l of light
Ref.
17
71
40
30
7
7
4
N/A
l 4 420 nm
l 4 420 nm
450 nm
447 nm
78
78
82
83
This journal is © The Royal Society of Chemistry 2015
View Article Online
Energy & Environmental Science
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
6. Oxygen-tolerant catalytic surfaces
‘Catalytic surfaces’ is a broad term that we apply to heterogeneous
surfaces, nanoparticles and immobilised assemblies in this
perspective. Given their generally high stability and amenability
to widespread use, such surfaces have been able to produce large
amounts of H2 at rates rivalling those of enzymatic systems and
many new examples have recently emerged.15,103 The wide scope
for structural and geometric modification through methods
such as doping, nanostructuring or controlled deposition of
multifunctional layers has allowed rational surface design to
maximise catalytic turnover and stability.12,104,105 Their use
includes a few disadvantages however, as they have generally low
‘per atom activity’ and ascertaining the exact nature of the catalytically active site and mechanism can be difficult.
Heterogeneous surfaces are considerably less sensitive to O2
than molecular complexes and hydrogenases (presumably due to
the absence of fragile organic ligand frameworks) and many
proton reducing surfaces are active O2 reduction catalysts.106,107
New developments in this field are instead focused on increasing
catalytic selectivity for H2 evolution over O2 reduction in order to
maximise efficiency.
Surface engineering to exclude O2 diffusion to the active
catalyst seeks to defend catalytic surfaces from O2 entirely. One
example of O2 exclusion has been presented by Domen and
coworkers on a photocatalytic water-splitting particle consisting of a (Ga1xZnx)(N1xOx) photocatalyst loaded with Rh. O2 is
particularly problematic in these systems as the Rh is able to
catalyse the H2 and O2-consuming back reaction of water
splitting (the reverse of reaction 1).13 It was found that the
back reaction could be completely prevented through the use of
a Cr2O3 layer. When the Rh cocatalyst was coated with Cr2O3
the water-splitting activity was greatly enhanced as the Cr2O3
blocked O2 from diffusing to the Rh surface (Fig. 10a).108,109
This effect was confirmed through a voltammetric study of a
Cr2O3-coated Rh electrode, which showed complete loss of the
O2 reduction wave on Rh.110 Proton reduction activity still
remained and was only slightly diminished as a result of the
Cr2O3 layer blocking some catalytic sites on the Rh. This was
confirmed through infrared spectroscopy, which illustrated
that protons were able to penetrate the Cr2O3 to reach a
catalytic Pt surface.
Fig. 10 (a) Schematic representation of O2 exclusion by a Cr2O3 layer
loaded on a Rh cocatalyst for photocatalytic H2 production.110 (b) Illustration of O2-driven self-repair after photocorrosion of a CuRhO2 electrode
to form inactive Cu0.111
This journal is © The Royal Society of Chemistry 2015
Perspective
A similar strategy has been utilised by Dey and coworkers
using ammonium tetrathiomolybdate (ATM),112 a reagent commonly used as a precursor to H2-evolving MoSx. It was proposed
that the ATM formed a layer on Au that could shuttle protons,
whilst preventing access of O2 to catalytically active sites. CV of
an ATM-Au electrode showed no O2 reduction wave and CPE
with 180 mV applied overpotential under air gave a high FE of
89% for proton reduction over 10 hours. The oxygen tolerance
of the MoSx archetype is believed to originate from the S ligand,
which plays a key role in the proton reduction mechanism.103
A number of other surface coatings have been able to
prevent O2 reduction at photocatalyst surfaces, such as: lanthanide oxide layers based on La, Pr, Sm, Gd, and Dy on Rh loaded
(Ga1xZnx)(N1xOx);113 amorphous Si and Ti oxyhydroxides on
perovskite-type oxynitride, LaMgxTa1xO1+3xN23x (x Z 1/3);114
surface-corroded Ti4+-doped Fe2O3;115 electrodeposited amorphous
TiO2 on W-doped BiVO4;116 NiO-loaded on NaTaO3117 and
cocatalysts of Au or RuO2.12,118 O2-excluding SiO2 layers for
electrocatalytic CO2 reduction have also emerged119 and the
presence of Li+ counter ions over K+ or Na+ has been shown to
assist in the preclusion of O2 reduction.120
Other strategies to prevent a catalyst from O2 interaction may
be achievable through O2-impermeable polymers. Research in
this field is well-established due to its amenability to industrial
applications, such as O2-impermeable packaging materials. A
number of polymer layers are generally impermeable to O2 and
thin coatings of metal oxides such as ZnO/SiOx and Al can lower
the O2 permeability further.121
Preventing O2 reduction can also be achieved through use of
selective catalysts. Takanabe and coworkers have synthesised
tungsten carbide nanoparticle cocatalysts that illustrate an
affinity for proton reduction over O2 reduction catalysis.122
Loading the nanoparticles onto a Na-doped SrTiO3 photocatalyst
increased H2-evolution activity and prevented O2 reduction,
which led to the UV light-driven production of stoichiometric
quantities of H2 and O2 through water splitting.
Alternatively, O2 in solution can be used to maintain a
catalytic structure through O2-driven self-repair. This has been
demonstrated by Bocarsly and coworkers using a delafossite
CuRhO2 structured electrode that functions most effectively
under air (Fig. 10b).111 O2-driven self-repair is a form of O2
tolerance that reduces O2 to regenerate the active catalytic
material. CuRhO2 is a photocathode for proton reduction at
an applied bias of 0.7 V vs. NHE in 1 M NaOH. Under inert
atmospheres the surface is active for 3 hours of photoelectrolysis, whereas in an aerobic atmosphere the activity remained
constant over 8 hours. The increased stability in the presence of
O2 was proven via X-ray photoelectron spectroscopy to be a
result of regeneration of CuI by dissolved O2, which precluded
the accumulation of Cu0 deposits on the surface. The material
had a lowered FE compared to surfaces under inert atmospheres, at 80%, however this number is respectable in such
challenging conditions and the lost efficiency is merely a result
of the O2 reduction necessary for electrode regeneration.
In a similar example to the delafossite electrode above, a
CuFeO2 electrode presented by Choi and coworkers was more
Energy Environ. Sci.
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Perspective
stable in the presence of O2.123 The surface was able to produce
H2 under visible light with a very large applied bias of 1.4 V vs.
NHE in O2-saturated 1 M NaOH. The electrode had a photon to
current ratio of 2.2% under Ar saturated and 3.7% under O2
saturated solutions suggesting that the electrode was less
selective towards H2 evolution than CuRhO2. This has since
been followed up by the Sivula group who described a sol–gel
technique to fabricate a similar electrode,124 which was further
doped with O2 to improve performance.
Heterogeneous, proton-reducing surfaces offer the most
simple and robust strategies to achieve O2-tolerant H2 evolution. The use of O2-excluding layers is particularly interesting as
the approach is also amenable to the systems discussed in
Sections 4 and 5 of this perspective. It should be noted that it is
still rare for H2 evolution activity to be studied under aerobic
conditions and more studies of the presented strategies in the
presence of O2 are therefore necessary.
7. Conclusion and future outlook
This perspective describes the state-of-the-art for the rapidly
developing field of O2-tolerant proton reduction catalysis. Each
of the catalytic classes discussed in Sections 4 to 6 demonstrate
distinct approaches to achieve aerobic proton reduction, which
revolve around either a defensive or an offensive strategy
(Fig. 11). Future advances will surely involve a combined use
of such techniques across enzymatic, molecular and surfacebased catalysts, which we hope to bring together in this work.
Defensive methods to preclude O2 inhibition will allow the
use of O2-sensitive catalysts under less stringent conditions. The
use of O2 shields offers a simple and effective approach to remove
O2, but such systems do not ensure complete elimination of O2
Energy & Environmental Science
from a system and greatly lower catalytic efficiency. O2-exclusion
layers are in theory a more effective route for O2-sensitive systems
as they generate an anaerobic environment for catalysis without
reducing the overall efficiency. These would be particularly useful
for highly O2-sensitive catalysts, such as hydrogenases.
Offensive techniques utilise the catalytic centre to remove O2
from solution without damaging the catalyst and will be much
simpler to utilise on a large scale. O2 tolerance has been identified in
a number of catalysts and although not formally tested, is presumably present in a number of other species. O2 tolerance results in a
lowered efficiency for proton reduction and decreasing the catalytic
affinity for O2 reduction is therefore the predominant issue to be
solved. O2-tolerant systems can be further optimised through combination with defensive strategies, such as O2-exclusion layers. Alternatively O2 can be used to improve the stability of reductively
corroded catalysts through O2-driven self-repair, taking advantage
of oxidising aerobic atmospheres. This has proven particularly useful
for delafossite structured catalysts and may also prove effective for
other catalysts that decompose in inert atmospheres.
To make further progress in this field it is important that O2
inhibition becomes a more common test of a proton reduction
system. A tolerance to O2 is an excellent trait for a catalyst to exhibit
and should be reported alongside other catalytic properties. Establishing the impact of O2 is simple; a catalyst’s interaction with O2 can
be studied with an extra electrolysis or photolysis experiment under
aerobic conditions rather than an inert atmosphere.
More in depth studies of O2-tolerant catalyst systems should also
become commonplace. Future studies would benefit from the use of
rotating ring-disk electrodes and quantification of the produced ROS
to help gain a better understanding of catalytic behaviour and
deactivation pathways under air. Appreciating the factors that contribute to proton reduction inhibition by O2 should then pave the
way for water splitting systems capable of functioning flawlessly
under aerobic conditions. Whether such a system would be best
implemented with an enzymatic, molecular or surface-based catalyst
is yet to be determined, however the chemical strategies used to
avoid O2 inhibition can mutually benefit the field as a whole.
The strategies considered in this perspective are also applicable
to the production of other renewable fuels. Catalytic processes, such
as CO2 reduction, offer alternate routes to artificial photosynthesis
and would similarly benefit from O2-tolerant catalysts (for high
aerobic stability) in combination with O2-exclusion strategies (for
high efficiency). There are also other inhibitors to investigate, such
as CO, which is formed in synthesis gas producing systems or
through unwanted side reactions (e.g. in formic acid decomposition),
the impact of which is seldom explored.79 Understanding inhibition
across a range of inhibitors and catalytic processes will have the dual
benefit of increasing our understanding of catalytic active sites and
increasing the viability of each system to more widespread production of sustainable, pollution-free fuel.
Acknowledgements
Fig. 11 A summary of the offensive/defensive strategies used to evolve H2
in the presence of O2.
Energy Environ. Sci.
Financial support from the EPSRC (EP/H00338X/2), the Christian Doppler Research Association (Austrian Federal Ministry of
This journal is © The Royal Society of Chemistry 2015
View Article Online
Energy & Environmental Science
Science, Research and Economy and National Foundation for
Research, Technology and Development), and the OMV Group
is gratefully acknowledged. Further thanks are extended to Mr
Timothy E. Rosser, Dr Chong-Yong Lee and Dr Hyun S. Park for
useful comments and fruitful discussions.
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Notes and references
1 J. Barber, Chem. Soc. Rev., 2009, 38, 185–196.
2 Y. Tachibana, L. Vayssieres and J. R. Durrant, Nat. Photonics,
2012, 6, 511–518.
3 C.-Y. Lin, D. Mersch, D. A. Jefferson and E. Reisner, Chem.
Sci., 2014, 5, 4906–4913.
4 V. S. Thoi, Y. Sun, J. R. Long and C. J. Chang, Chem. Soc.
Rev., 2013, 42, 2388–2400.
5 W. T. Eckenhoff and R. Eisenberg, Dalton Trans., 2012, 41,
13004–13021.
6 F. E. Osterloh, J. Phys. Chem. Lett., 2014, 5, 2510–2511.
7 C.-Y. Lin, Y.-H. Lai, D. Mersch and E. Reisner, Chem. Sci.,
2012, 3, 3482–3487.
8 L. Ghassemzadeh, K.-D. Kreuer, J. Maier and K. Müller,
J. Phys. Chem. C, 2010, 114, 14635–14645.
9 M. Danilczuk, F. D. Coms and S. Schlick, J. Phys. Chem. B,
2009, 113, 8031–8042.
10 D. G. Nocera, Acc. Chem. Res., 2012, 45, 767–776.
11 R. E. Rocheleau, E. L. Miller and A. Misra, Energy Fuels,
1998, 12, 3–10.
12 A. Kudo and Y. Miseki, Chem. Soc. Rev., 2009, 38, 253–278.
13 K. Maeda and K. Domen, J. Phys. Chem. Lett., 2010, 1,
2655–2661.
14 W. Lubitz, H. Ogata, O. Rüdiger and E. Reijerse, Chem.
Rev., 2014, 114, 4081–4148.
15 P. C. K. Vesborg, B. Seger and I. Chorkendorff, J. Phys.
Chem. Lett., 2015, 6, 951–957.
16 C. C. L. McCrory, S. Jung, I. M. Ferrer, S. M. Chatman,
J. C. Peters and T. F. Jaramillo, J. Am. Chem. Soc., 2015, 137,
4347–4357.
17 P. M. Wood, Biochem. J., 1988, 253, 287–289.
18 A. A. Gewirth and M. S. Thorum, Inorg. Chem., 2010, 49,
3557–3566.
19 C. Costentin, S. Drouet, M. Robert and J.-M. Savéant, J. Am.
Chem. Soc., 2012, 134, 11235–11242.
20 A. J. Bard and L. R. Faulkner, Electrochemical Methods: Fundamentals and Applications, Wiley, New York, 2nd edn, 2001.
21 Electrochemical measurements were carried out on a
potentiostat (Ivium) with a Ag/AgCl reference electrode
(sat. KCl, BASi) and a platinum-mesh counter electrode.
Potentials were converted to NHE through the relationship: E (V) vs. NHE = E (V) vs. Ag/AgCl + 0.197 V.
22 J. Zhao and F. E. Osterloh, J. Phys. Chem. Lett., 2014, 5, 782–786.
23 E. Yeager, Electrochim. Acta, 1984, 29, 1527–1537.
24 N. Kaeffer, A. Morozan and V. Artero, J. Phys. Chem. B,
2015, DOI: 10.1021/acs.jpcb.5b03136.
25 Y. Tian, L. Mao, T. Okajima and T. Ohsaka, Anal. Chem.,
2002, 74, 2428–2434.
This journal is © The Royal Society of Chemistry 2015
Perspective
26 L. Campanella, G. Favero and M. Tomassetti, Anal. Lett.,
1999, 32, 2559–2581.
27 M. I. Song, F. F. Bier and F. W. Scheller, Bioelectrochem.
Bioenerg., 1995, 38, 419–422.
28 K. Tammeveski, T. T. Tenno, A. A. Mashirin, E. W. Hillhouse,
P. Manning and C. J. McNeil, Free Radical Biol. Med., 1998, 25,
973–978.
29 W. Scheller, W. Jin, E. Ehrentreich-Förster, B. Ge, F. Lisdat,
R. Büttemeier, U. Wollenberger and F. W. Scheller, Electroanalysis, 1999, 11, 703–706.
30 H. Flamm, J. Kieninger, A. Weltin and G. A. Urban, Biosens.
Bioelectron., 2015, 65, 354–359.
31 X. J. Chen, A. C. West, D. M. Cropek and S. Banta, Anal.
Chem., 2008, 80, 9622–9629.
32 S. Madhurantakam, S. Selvaraj, N. Nesakumar, S. Sethuraman,
J. B. B. Rayappan and U. M. Krishnan, Biosens. Bioelectron.,
2014, 59, 134–139.
33 Q. Zhang, Y. Qiao, L. Zhang, S. Wu, H. Zhou, J. Xu and
X.-M. Song, Electroanalysis, 2011, 23, 900–906.
34 C. Xiang, Y. Zou, L.-X. Sun and F. Xu, Electrochem. Commun.,
2008, 10, 38–41.
35 J. Bai and X. Jiang, Anal. Chem., 2013, 85, 8095–8101.
36 C. Calas-Blanchard, G. Catanante and T. Noguer, Electroanalysis, 2014, 26, 1277–1286.
37 J. M. Burns, W. J. Cooper, J. L. Ferry, D. W. King,
B. P. DiMento, K. McNeill, C. J. Miller, W. L. Miller,
B. M. Peake, S. A. Rusak, A. L. Rose and T. D. Waite, Aquat.
Sci., 2012, 74, 683–734.
38 G. Bartosz, Clin. Chim. Acta, 2006, 368, 53–76.
39 P. M. Vignais and B. Billoud, Chem. Rev., 2007, 107, 4206–4272.
40 A. K. Jones, E. Sillery, S. P. J. Albracht and F. A. Armstrong,
Chem. Commun., 2002, 866–867.
41 M.-E. Pandelia, H. Ogata and W. Lubitz, ChemPhysChem,
2010, 11, 1127–1140.
42 B. Friedrich, J. Fritsch and O. Lenz, Curr. Opin. Biotechnol.,
2011, 22, 358–364.
43 F. A. Armstrong, N. A. Belsey, J. A. Cracknell, G. Goldet,
A. Parkin, E. Reisner, K. A. Vincent and A. F. Wait, Chem.
Soc. Rev., 2009, 38, 36–51.
44 S. T. Stripp, G. Goldet, C. Brandmayr, O. Sanganas, K. A.
Vincent, M. Haumann, F. A. Armstrong and T. Happe, Proc.
Natl. Acad. Sci. U. S. A., 2009, 106, 17331–17336.
45 H. Ogata, S. Hirota, A. Nakahara, H. Komori, N. Shibata,
T. Kato, K. Kano and Y. Higuchi, Structure, 2005, 13,
1635–1642.
46 A. Volbeda, L. Martin, C. Cavazza, M. Matho, B. W. Faber,
W. Roseboom, S. P. J. Albracht, E. Garcin, M. Rousset and
J. C. Fontecilla-Camps, J. Biol. Inorg. Chem., 2005, 10, 239–249.
47 L. Lauterbach and O. Lenz, J. Am. Chem. Soc., 2013, 135,
17897–17905.
48 T. Burgdorf, O. Lenz, T. Buhrke, E. van der Linden,
A. K. Jones, S. P. J. Albracht and B. Friedrich, J. Mol.
Microbiol. Biotechnol., 2005, 10, 181–196.
49 G. Goldet, A. F. Wait, J. A. Cracknell, K. A. Vincent,
M. Ludwig, O. Lenz, B. Friedrich and F. A. Armstrong,
J. Am. Chem. Soc., 2008, 130, 11106–11113.
Energy Environ. Sci.
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Perspective
50 J. Fritsch, P. Scheerer, S. Frielingsdorf, S. Kroschinsky,
B. Friedrich, O. Lenz and C. M. T. Spahn, Nature, 2011,
479, 249–252.
51 A. Volbeda, P. Amara, C. Darnault, J.-M. Mouesca, A. Parkin,
M. M. Roessler, F. A. Armstrong and J. C. Fontecilla-Camps,
Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 5305–5310.
52 Y. Shomura, K.-S. Yoon, H. Nishihara and Y. Higuchi,
Nature, 2011, 479, 253–256.
53 M. Horch, L. Lauterbach, M. A. Mroginski, P. Hildebrandt,
O. Lenz and I. Zebger, J. Am. Chem. Soc., 2015, 137,
2555–2564.
54 A. Volbeda, P. Amara, M. Iannello, A. L. De Lacey,
C. Cavazza and J. C. Fontecilla-Camps, Chem. Commun.,
2013, 49, 7061–7063.
55 M. C. Marques, R. Coelho, I. A. C. Pereira and P. M. Matias,
Int. J. Hydrogen Energy, 2013, 38, 8664–8682.
56 M. C. Marques, R. Coelho, A. L. De Lacey, I. A. C. Pereira
and P. M. Matias, J. Mol. Biol., 2010, 396, 893–907.
57 C. Wombwell and E. Reisner, Chem. – Eur. J., 2015, 21,
8096–8104.
58 M. Teixeira, G. Fauque, I. Moura, P. A. Lespinat, Y. Berlier,
B. Prickril, H. D. Peck Jr., A. V. Xavier, J. Le Gall and
J. J. G. Moura, Eur. J. Biochem., 1987, 167, 47–58.
59 O. Skaff, D. I. Pattison, P. E. Morgan, R. Bachana,
V. K. Jain, K. I. Priyadarsini and M. J. Davies, Biochem. J.,
2012, 441, 305–316.
60 V. Radu, S. Frielingsdorf, S. D. Evans, O. Lenz and
L. J. C. Jeuken, J. Am. Chem. Soc., 2014, 136, 8512–8515.
61 S. V. Hexter, F. Grey, T. Happe, V. Climent and F. A. Armstrong,
Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 11516–11521.
62 T. Sakai, D. Mersch and E. Reisner, Angew. Chem., Int. Ed.,
2013, 52, 12313–12316.
63 T. Noji, M. Kondo, T. Jin, T. Yazawa, H. Osuka, Y. Higuchi,
M. Nango, S. Itoh and T. Dewa, J. Phys. Chem. Lett., 2014, 5,
2402–2407.
64 E. Reisner, D. J. Powell, C. Cavazza, J. C. Fontecilla-Camps
and F. A. Armstrong, J. Am. Chem. Soc., 2009, 131,
18457–18466.
65 O. A. Zadvornyy, J. E. Lucon, R. Gerlach, N. A. Zorin,
T. Douglas, T. E. Elgren and J. W. Peters, J. Inorg. Biochem.,
2012, 106, 151–155.
66 A. P. Gerola, J. Semensato, D. S. Pellosi, V. R. Batistela,
B. R. Rabello, N. Hioka and W. Caetano, J. Photochem.
Photobiol., A, 2012, 232, 14–21.
67 S. V. Morozov, O. G. Voronin, E. E. Karyakina, N. A. Zorin,
S. Cosnier and A. A. Karyakin, Electrochem. Commun., 2006,
8, 851–854.
68 N. Plumeré, O. Rüdiger, A. A. Oughli, R. Williams,
J. Vivekananthan, S. Pöller, W. Schuhmann and
W. Lubitz, Nat. Chem., 2014, 6, 822–827.
69 L. Xu and F. A. Armstrong, RSC Adv., 2015, 5, 3649–3656.
70 C. Tard and C. J. Pickett, Chem. Rev., 2009, 109, 2245–2274.
71 H. I. Karunadasa, E. Montalvo, Y. Sun, M. Majda, J. R. Long
and C. J. Chang, Science, 2012, 335, 698–702.
72 M. L. Helm, M. P. Stewart, R. M. Bullock, M. Rakowski
DuBois and D. L. DuBois, Science, 2011, 333, 863–866.
Energy Environ. Sci.
Energy & Environmental Science
73 W. R. McNamara, Z. Han, P. J. Alperin, W. W. Brennessel,
P. L. Holland and R. Eisenberg, J. Am. Chem. Soc., 2011,
133, 15368–15371.
74 Z. Han, W. R. McNamara, M.-S. Eum, P. L. Holland and
R. Eisenberg, Angew. Chem., Int. Ed., 2012, 51, 1667–1670.
75 M. A. Gross, A. Reynal, J. R. Durrant and E. Reisner, J. Am.
Chem. Soc., 2014, 136, 356–366.
76 T. S. Teets and D. G. Nocera, Chem. Commun., 2011, 47,
9268–9274.
77 G. Caserta, S. Roy, M. Atta, V. Artero and M. Fontecave,
Curr. Opin. Chem. Biol., 2015, 25, 36–47.
78 F. Lakadamyali, M. Kato, N. M. Muresan and E. Reisner,
Angew. Chem., Int. Ed., 2012, 51, 9381–9384.
79 D. W. Wakerley, M. A. Gross and E. Reisner, Chem. Commun.,
2014, 50, 15995–15998.
80 B. Mondal, K. Sengupta, A. Rana, A. Mahammed,
M. Botoshansky, S. G. Dey, Z. Gross and A. Dey, Inorg.
Chem., 2013, 52, 3381–3387.
81 J. G. Kleingardner, B. Kandemir and K. L. Bren, J. Am.
Chem. Soc., 2014, 136, 4–7.
82 W. M. Singh, T. Baine, S. Kudo, S. Tian, X. A. N. Ma,
H. Zhou, N. J. DeYonker, T. C. Pham, J. C. Bollinger,
D. L. Baker, B. Yan, C. E. Webster and X. Zhao, Angew.
Chem., Int. Ed., 2012, 51, 5941–5944.
83 A. Call, Z. Codolà, F. Acuña-Parés and J. Lloret-Fillol,
Chem. – Eur. J., 2014, 20, 6171–6183.
84 D. W. Wakerley and E. Reisner, Phys. Chem. Chem. Phys.,
2014, 16, 5739–5746.
85 S. Ji, W. Wu, W. Wu, P. Song, K. Han, Z. Wang, S. Liu,
H. Guo and J. Zhao, J. Mater. Chem., 2010, 20, 1953–1963.
86 Y.-F. Li and A. Selloni, J. Am. Chem. Soc., 2013, 135, 9195–9199.
87 K. Hanson, M. K. Brennaman, H. Luo, C. R. K. Glasson,
J. J. Concepcion, W. Song and T. J. Meyer, ACS Appl. Mater.
Interfaces, 2012, 4, 1462–1469.
88 A. Schechter, M. Stanevsky, A. Mahammed and Z. Gross,
Inorg. Chem., 2012, 51, 22–24.
89 R. Sander, Atmos. Chem. Phys. Discuss., 2014, 14,
29615–30521.
90 P. Han and D. M. Bartels, J. Phys. Chem., 1996, 100,
5597–5602.
91 Y. Sun, J. P. Bigi, N. A. Piro, M. L. Tang, J. R. Long and
C. J. Chang, J. Am. Chem. Soc., 2011, 133, 9212–9215.
92 R. S. Khnayzer, V. S. Thoi, M. Nippe, A. E. King, J. W. Jurss,
K. A. El Roz, J. R. Long, C. J. Chang and F. N. Castellano,
Energy Environ. Sci., 2014, 7, 1477–1488.
93 M. Razavet, V. Artero and M. Fontecave, Inorg. Chem., 2005,
44, 4786–4795.
94 R. M. Kellett and T. G. Spiro, Inorg. Chem., 1985, 24,
2373–2377.
95 G. N. Schrauzer and L. P. Lee, J. Am. Chem. Soc., 1970, 92,
1551–1557.
96 G. N. Schrauzer, Angew. Chem., Int. Ed., 1976, 15, 417–426.
97 M. Shamsipur, A. Salimi, H. Haddadzadeh and M. F. Mousavi,
J. Electroanal. Chem., 2001, 517, 37–44.
98 J. L. Dempsey, B. S. Brunschwig, J. R. Winkler and
H. B. Gray, Acc. Chem. Res., 2009, 42, 1995–2004.
This journal is © The Royal Society of Chemistry 2015
View Article Online
Open Access Article. Published on 29 May 2015. Downloaded on 19/06/2015 14:49:25.
This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.
Energy & Environmental Science
99 J. Y. Yang, R. M. Bullock, W. G. Dougherty, W. S. Kassel,
B. Twamley, D. L. DuBois and M. Rakowski DuBois, Dalton
Trans., 2010, 39, 3001–3010.
100 A. Das, Z. Han, W. W. Brennessel, P. L. Holland and
R. Eisenberg, ACS Catal., 2015, 5, 1397–1406.
101 J. M. Achord and C. L. Hussey, Anal. Chem., 1980, 52, 601–602.
102 P. H.-L. Sit, R. Car, M. H. Cohen and A. Selloni, Proc. Natl.
Acad. Sci. U. S. A., 2013, 110, 2017–2022.
103 D. Merki and X. Hu, Energy Environ. Sci., 2011, 4, 3878–3888.
104 M. P. Soriaga, J. H. Baricuatro, K. D. Cummins, Y.-G. Kim, F. H.
Saadi, G. Sun, C. C. L. McCrory, J. R. McKone, J. M. Velazquez,
I. M. Ferrer, A. I. Carim, A. Javier, B. Chmielowiec, D. C. Lacy,
J. M. Gregoire, J. Sanabria-Chinchilla, X. Amashukeli,
W. J. Royea, B. S. Brunschwig, J. C. Hemminger, N. S. Lewis
and J. L. Stickney, Surf. Sci., 2015, 631, 285–294.
105 Y. Ma, X. Wang, Y. Jia, X. Chen, H. Han and C. Li, Chem.
Rev., 2014, 114, 9987–10043.
106 T. Wang, D. Gao, J. Zhuo, Z. Zhu, P. Papakonstantinou,
Y. Li and M. Li, Chem. – Eur. J., 2013, 19, 11939–11948.
107 Y. Wang, E. Laborda, K. Tschulik, C. Damm, A. Molina and
R. G. Compton, Nanoscale, 2014, 6, 11024–11030.
108 K. Maeda, K. Teramura, D. Lu, N. Saito, Y. Inoue and
K. Domen, Angew. Chem., Int. Ed., 2006, 45, 7806–7809.
109 K. Maeda, K. Teramura, D. Lu, N. Saito, Y. Inoue and
K. Domen, J. Phys. Chem. C, 2007, 111, 7554–7560.
110 M. Yoshida, K. Takanabe, K. Maeda, A. Ishikawa, J. Kubota,
Y. Sakata, Y. Ikezawa and K. Domen, J. Phys. Chem. C, 2009,
113, 10151–10157.
This journal is © The Royal Society of Chemistry 2015
Perspective
111 J. Gu, Y. Yan, J. W. Krizan, Q. D. Gibson, Z. M. Detweiler,
R. J. Cava and A. B. Bocarsly, J. Am. Chem. Soc., 2014, 136,
830–833.
112 S. Chatterjee, K. Sengupta, S. Dey and A. Dey, Inorg. Chem.,
2013, 52, 14168–14177.
113 M. Yoshida, K. Maeda, D. Lu, J. Kubota and K. Domen,
J. Phys. Chem. C, 2013, 117, 14000–14006.
114 C. Pan, T. Takata, M. Nakabayashi, T. Matsumoto,
N. Shibata, Y. Ikuhara and K. Domen, Angew. Chem., Int.
Ed., 2015, 54, 2955–2959.
115 D. Cao, W. Luo, J. Feng, X. Zhao, Z. Li and Z. Zou, Energy
Environ. Sci., 2014, 7, 752–759.
116 D. Eisenberg, H. S. Ahn and A. J. Bard, J. Am. Chem. Soc.,
2014, 136, 14011–14014.
117 Y. Matsumoto, U. Unal, N. Tanaka, A. Kudo and H. Kato,
J. Solid State Chem., 2004, 177, 4205–4212.
118 A. Iwase, H. Kato and A. Kudo, Catal. Lett., 2006, 108, 7–10.
119 G. Yuan, A. Agiral, N. Pellet, W. Kim and H. Frei, Faraday
Discuss., 2014, 176, 233–249.
120 C. Ding, X. Zhou, J. Shi, P. Yan, Z. Wang, G. Liu and C. Li,
J. Phys. Chem. B, 2015, 119, 3560–3566.
121 Y. Leterrier, Prog. Mater. Sci., 2003, 48, 1–55.
122 A. T. Garcia-Esparza, D. Cha, Y. Ou, J. Kubota, K. Domen
and K. Takanabe, ChemSusChem, 2013, 6, 168–181.
123 C. G. Read, Y. Park and K.-S. Choi, J. Phys. Chem. Lett.,
2012, 3, 1872–1876.
124 M. S. Prévot, N. Guijarro and K. Sivula, ChemSusChem,
2015, 8, 1359–1367.
Energy Environ. Sci.